Identification and biologic significance of micrometastases in axillary lymph nodes in patients with invasive breast cancer

Archives of Pathology and Laboratory Medicine

Volumn 133, Issue 6, 2009, Pages 869-878

  Sahin, Aysegul A ^a   Guray, Merih ^a   Hunt, Kelly K ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER; CANCER GROWTH; CANCER INVASION; CANCER RISK; CANCER SURVIVAL; CLINICAL EVALUATION; CLINICAL FEATURE; HUMAN; IMMUNOHISTOCHEMISTRY; REVIEW; SENTINEL LYMPH NODE BIOPSY;

BREAST NEOPLASMS; FEMALE; HUMANS; LYMPHATIC METASTASIS; PRACTICE GUIDELINES AS TOPIC; PROGNOSIS; SENTINEL LYMPH NODE BIOPSY;

EID: 67049171226     PISSN: 00039985     EISSN: 15432165     Source Type: Journal    
DOI: None     Document Type: Review

References (103)

1. Fitzgibbons PL, Page DL, Weaver D, et al. Prognostic factors in breast cancer: College of American Pathologists Consensus Statement 1999. Arch Pathol Lab Med. 2000;124:966-978.
2. Saez RA, McGuire WL, Clark CM. Prognostic factors in breast cancer. Semin Surg Oncol. 1989;5:102-110. (Pubitemid 19130774)
3. van der Ploeg IM, Nieweg OE, van Rijk MC, Valdés Olmos RA, Kroon BB. Axillary recurrence after a tumour-negative sentinel node biopsy in breast cancer patients: a systematic review and meta-analysis of the literature. Eur J Surg Oncol. 2008;34:1277-1284.
4. Giuliano AE, Kirgan DM, Guenther JM, Morton DL. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg. 1994;220:391-401. (Pubitemid 24313232)
5. Veronesi U, Paganelli G, Viale G, et al. A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med. 2003;349:546-553. (Pubitemid 36951366)
6. Krag DN, Julian TB, Harlow SP, et al. NSABP-32: phase III, randomized trial comparing axillary resection with sentinel node dissection: a description of the trial. Ann Surg Oncol. 2004;11:208S-210S.
7. Mansel RE, Fallowwfield L, Kissin M, et al. Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC Trial. J Natl Cancer Inst. 2006;98:599-609. (Pubitemid 43904843)
8. Purushotham AD, Upponi S, Klevesath MB, et al. Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial. J Clin Oncol. 2005;23:4312-4321. (Pubitemid 46209968)
9. Samphao S, Eremin JM, El-Sheemy M, Eremin O. Management of the axilla in women with breast cancer: current clinical practice and a new selective targeted approach. Ann Surg Oncol. 2008;15:1282-1296.
10. Lyman GH, Giuliano AE, Somerfield MR, et al. American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. J Clin Oncol. 2005;23:7703-7720. (Pubitemid 46291835)
11. Giuliano AE, Kirgan DM, Guenther JM, et al. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg. 1994;220:391-401. (Pubitemid 24313232)
12. Giuliano AE. Sentinel lymphadenectomy in primary breast carcinoma: an alternative to routine axillary dissection. J Surg Oncol. 1996;62:75-77. (Pubitemid 26196502)
13. Greene FL, Page DL, Fleming ID, et al, eds. Breast. In: American Joint Committee on Cancer Staging Manual. 6th ed. New York, New York: Springer-Verlag; 2002:223-240.
14. Grabau D. Breast cancer patients with micrometastases only: is a basis provided for tailored treatment? Surg Oncol. 2008;17:211-217.
15. Patani N, Mokbel K. The clinical significance of sentinel lymph node micrometastasis in breast cancer. Breast Cancer Res Treat. 2009;114:393-402.
16. Mittendorf EA, Hunt KK. Significance and management of micrometastases in patients with breast cancer. Expert Rev Anticancer Ther. 2007;7:1451-1461. (Pubitemid 351826910)
17. Wada N, Imoto S. Clinical evidence of breast cancer micrometastasis in the era of sentinel node biopsy. Int J Clin Oncol. 2008;13:24-32. (Pubitemid 351326290)
18. Huvos AG, Hutter RVP, Berg JW. Significance of axillary macrometastases and micrometastases in mammary cancer. Ann Surg. 1971;173:44-46.
19. Singletary SE, Allred C, Ashley P, et al. Revision of the American Joint Committee on Cancer staging system for breast cancer. J Clin Oncol. 2002;20:3628-3636. (Pubitemid 34983222)
20. Singletary SE, Greene FL, Sobin LH. Classification of isolated tumor cells: clarification of the 6th edition of the American Joint Committee on Cancer Staging Manual. Cancer. 2003;98:2740-2741. (Pubitemid 37509544)
21. Singletary SE, Connolly JL. Breast cancer staging: working with the sixth edition of the AJCC Cancer Staging Manual. CA Cancer J Clin. 2006;56:37-47. (Pubitemid 43228386)
22. Friedman S, Bertin F, Mouriesse H, et al. Importance of tumor cells in axillary node sinus margins ('clandestine' metastases) discovered by serial sectioning in operable breast carcinoma. Acta Oncol. 1988;27:483-487. (Pubitemid 19013277)
23. Pickren JW. Significance of occult metastases: a study of breast cancer. Cancer. 1961;14:1266-1271.
24. Fisher ER, Swamidoss S, Lee CH, Rockette H, Redmond C, Fisher B. Detection and significance of occult axillary node metastases in patients with invasive breast cancer. Cancer. 1978;42:2025-2031. (Pubitemid 9055971)
25. Wilkinson EJ, Hause LL, Hoffman RG, et al. Occult axillary lymph node metastases in invasive breast carcinoma: characteristics of the primary tumor and significance of the metastases. Pathol Annu. 1982;17:67-91.
26. Zhang PJ, Reisner RM, Nangia R, Edge SB, Brooks JJ. Effectiveness of multiple-level sectioning in detecting axillary nodal micrometastasis in breast cancer: a retrospective study with immunohistochemical analysis. Arch Pathol Lab Med. 1998;122:687-690. (Pubitemid 28364135)
27. International (Ludwig) Breast Cancer Study Group. Prognostic importance of occult axillary lymph node micrometastases from breast cancers. Lancet. 1990;335:1565-1568. (Pubitemid 20189634)
28. Hainsworth PJ, Tjandra JJ, Stillwell RG, et al. Detection and significance of occult metastases in node-negative breast cancer. Br J Surg. 1993;80:459-463. (Pubitemid 23116083)
29. de Mascarel I, MacGrogan G, Picot V, Mathoulin-Pelissier S. Prognostic significance of immunohistochemically detected breast cancer node metastases in 218 patients. Br J Cancer. 2002;87:70-74. (Pubitemid 34888606)
30. Reed W, Bohler PJ, Sandstad B, Nesland JM. Occult metastases in axillary lymph nodes as a predictor of survival in node-negative breast carcinoma with long-term follow-up. Breast J. 2004;10:174-180. (Pubitemid 38715730)
31. Cote RJ, Peterson HF, Chaiwun B, et al. Role of immunohistochemical detection of lymph-node metastases in management of breast cancer: International Breast Cancer Study Group. Lancet. 1999;354:896-900.
32. McGuckin MA, Cummings MC, Walsh MD, Hohn BG, Bennett IC, Wright RG. Occult axillary node metastases in breast cancer: their detection and prognostic significance. Br J Cancer. 1996;73:88-95. (Pubitemid 26026266)
33. Chu KU, Turner RR, Hansen NM, Brennan MB, Giuliano AE. Sentinel node metastasis in patients with breast carcinoma accurately predicts immunohistochemically detectable nonsentinel node metastasis. Ann Surg Oncol. 1999;6:756-761. (Pubitemid 30013652)
34. Czerniecki BJ, Scheff AM, Callans LS, et al. Immunohistochemistry with pancytokeratins improves the sensitivity of sentinel lymph node biopsy in patients with breast carcinoma. Cancer. 1999;85:1098-1103. (Pubitemid 29115589)
35. Noguchi S. The detection of breast cancer micrometastases in axillary lymph nodes by means of reverse transcriptase polymerase chain reaction. Cancer. 1994;74:1595-1600. (Pubitemid 24302980)
36. Kurosumi M, Takei H. Significance and problems of histopathological examination and utility of real-time reverse transcriptase-polymerase chain reaction method for the detection of sentinel lymph node metastasis in breast cancer. Breast Cancer. 2007;14:342-349.
37. Lyman GH, Giuliano AE, Somerfield MR, et al. American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. J Clin Oncol. 2005;23:7703-7720. (Pubitemid 46291835)
38. Cserni G. A model for determining the optimum histology of sentinel lymph nodes in breast cancer. J Clin Pathol. 2004;57:467-471. (Pubitemid 38621790)
39. Schwartz GF, Giuliano AE, Veronesi U. Consensus Conference Committee: proceedings of consensus conference on the role of sentinel lymph node biopsy in carcinoma of the breast. Hum Pathol. 2002;23:579-589.
40. Pathology Reporting of Breast Disease: Cancer Screening Programs 2005. NHSBSP publication 58. http://cancerscreening.org.uk/breastscreen/publications/ nhsbsp58-low-resolution.pdf. Accessed October 28, 2008.
41. Perry N, Broeders M, Wolf C, et al, eds. European Guidelines for Quality Assurance in Breast Cancer Screening and Diagnosis. 4th ed. Luxembourg: European Communities; 2006.
42. Kuehn T, Bembenek A, Decker T, et al. A concept for the clinical implementation of sentinel lymph node biopsy in patient with breast carcinoma with special regard to quality assurance. Cancer. 2005;103:451-461.
43. Meyer JS. Sentinel lymph node biopsy: strategies for pathologic examination of the specimen. J Surg Oncol. 1998;69:212-218. (Pubitemid 29024564)
44. Treseler P. Pathologic examination of the sentinel lymph node: what is the best method? Breast J. 2006;12(5 suppl 2):143-151. (Pubitemid 44337461)
45. Millis RR, Springall R, Lee AH, Ryder K, Rytina ER, Fentiman IS. Occult axillary lymph node metastases are of no prognostic significance in breast cancer. Br J Cancer. 2002;86:396-401. (Pubitemid 34185124)
46. Noguchi S, Aihara T, Motomura K, et al. The detection of breast carcinoma micrometastases in axillary lymph nodes by means of reverse transcriptase-polymerase chain reaction. Am J Pathol. 1996;148:649-656.
47. Masuda N, Tamaki Y, Sakita I, et al. Clinical significance of micrometastases in axillary lymph nodes assessed by reverse transcription- polymerase chain reaction in breast cancer patients. Clin Cancer Res. 2000;6:4176-4185.
48. Gillanders WE, Mikhitarian K, Hebert R, et al. Molecular detection of micrometastatic breast cancer in histopathology-negative axillary lymph nodes correlates with traditional predictors of prognosis: an interim analysis of a prospective multi-institutional cohort study. Ann Surg. 2004;239:828-840. (Pubitemid 38669433)
49. Viale G, Dell'Orto P, Biasi MO, et al. Comparative evaluation of an extensive histopathologic examination and a real-time reverse-transcription- polymerase chain reaction assay for mammaglobin and cytokeratin 19 on axillary sentinel lymph nodes of breast carcinoma patients. Ann Surg. 2008;247:136-142.
50. Visser M, Jiwa M, Horstman A, et al. Intra-operative rapid diagnostic method based on CK19 mRNA expression for the detection of lymph node metastases in breast cancer. Int J Cancer. 2008;122:2562-2567. (Pubitemid 351590490)
51. Fisher B, Bauer M, Wickerham L, Redmond CK, Fisher ER. Relation of number of positive axillary nodes to the prognosis of patients with primary breast cancer: an NSABP update. Cancer. 1983;52:1551-1557.
52. Rosen PP, Saigo PE, Braun DW Jr, Weathers E, DePalo A. Predictors of recurrence in stage I (T1N0M0) breast carcinoma. Ann Surg. 1981;193:15-25.
53. Cummings MC, Walsh MD, Hohn BG, Bennett IC, Wright RG, McGuckin MA. Occult axillary lymph node metastases in breast cancer do matter: results of 10-year survival analysis. Am J Surg Pathol. 2002;26:1286-1295.
54. Kahn HJ, Hanna WM, Chapman JA, et al. Biological significance of occult micrometastases in histologically negative axillary lymph nodes in breast cancer patients using the recent American Joint Committee on Cancer breast cancer staging system. Breast J. 2006;12:294-301. (Pubitemid 43989974)
55. Neville AM, Price KN, Gelber RD, Goldhirsch A. Axillary node micrometastases and breast cancer. Lancet. 1991;337:1110.
56. Trojani M, de Mascarel I, Bonichon F, Coindre JM, Delsol G. Micrometastases to axillary lymph nodes from carcinoma of breast: detection by immunohistochemistry and prognostic significance. Br J Cancer. 1987;55:303-306. (Pubitemid 17036845)
57. de Mascarel I, Bonichon F, Coindre JM, Trojani M. Prognostic significance of breast cancer axillary lymph node micrometastases assessed by two special techniques: reevaluation with longer follow-up. Br J Cancer. 1992;66:523-527.
58. Cote RJ, Peterson HF, Chaiwun B, et al. Role of immunohistochemical detection of lymph-node metastases in management of breast cancer: International Breast Cancer Study Group. Lancet. 1999;354:896-900.
59. Dowlatshahi K, Fan M, Snider H, Habib F. Lymph node micrometastases from breast carcinoma: review the dilemma. Cancer. 1997;80:1188-1197. (Pubitemid 27407219)
60. Sakorafas GH, Geraghty J, Pavlakis G. The clinical significance of axillary lymph node micrometastases in breast cancer. Eur J Surg Oncol. 2004;30:807-816. (Pubitemid 39186065)
61. Maibenco DC, Dombi GW, Kau TY, Severson RK. Significance of micrometastases on the survival of women with T1 breast cancer. Cancer. 2006;107:1234-1239. (Pubitemid 44452771)
62. Chen SL, Hoehne FM, Giuliano AE. The prognostic significance of micrometastases in breast cancer: a SEER population based analysis. Ann Surg Oncol. 2007;14:3378-3384. (Pubitemid 350160103)
63. Kuijt GP, Voogd AC, van de Poll-Franse LV, et al. The prognostic significance of axillary lymph-node micrometastases in breast cancer patients. Eur J Surg Oncol. 2005;31:500-505. (Pubitemid 40724091)
64. Cserni G, Gregori D, Merletti F, et al. Meta-analysis of non-sentinel node metastases associated with micrometastatic sentinel nodes in breast cancer. Br J Surg. 2004;91:1245-1252. (Pubitemid 39331448)
65. Viale G, Maiorano E, Pruneri G, et al. Predicting the risk for additional axillary metastases in patients with breast carcinoma and positive sentinel node biopsy. Ann Surg. 2005;241:319-325.
66. Cserni G, Bianchi S, Vezzosi V, et al. Sentinel lymph node biopsy in staging small (up to 15 mm) breast carcinomas: results from a European multi-institutional study. Pathol Oncol Res. 2007;13:5-14. (Pubitemid 46883541)
67. van Deurzen CH, van HR, Hobblink MG, et al. Predictive value of tumor load in breast cancer sentinel lymph nodes for second echelon lymph node metastases. Cell Oncol. 2007;29:497-505. (Pubitemid 350136504)
68. Degnim AC, Griffith KA, Sabel MS, et al. Clinicopathologic features of metastasis in nonsentinel lymph nodes of breast carcinoma patients. Cancer. 2003;98:2307-2315. (Pubitemid 37466644)
69. Turner RR, Chu KU, Qi K, et al. Pathologic features associated with nonsentinel lymph node metastases in patients with metastatic breast carcinoma in a sentinel lymph node. Cancer. 2000;89:574-581. (Pubitemid 30640103)
70. Samoilova E, Davis JT, Hinson J, et al. Size of sentinel node tumor deposits and extent of axillary lymph node involvement: which breast cancer patients may benefit from less aggressive axillary dissection? Ann Surg Oncol. 2007;14:2221-2227. (Pubitemid 47174930)
71. Van Deurzen CHM, Seldenrijk CA, Koelemij R, et al. The microanatomic location of metastatic breast cancer in sentinel lymph nodes predicts nonsentinel node involvement. Ann Surg Oncol. 2008;15:1309-1315.
72. Goyal A, Douglas-Jones AG, Newcombe RG, et al. Effect of lymphatic tumor burden on sentinel lymph node biopsy in breast cancer. Breast J. 2005;11:188-194. (Pubitemid 40664062)
73. Cserni G. Axillary sentinel lymph node micrometastases with extracapsular extension: a distinct pattern of breast cancer metastasis? J Clin Pathol. 2008;61:115-118. (Pubitemid 351158236)
74. Starz H, Balda BR, Kramer KU, et al. A micromorphometry based concept for routine classification of sentinel lymph node metastases and its clinical relevance for patients with melanoma. Cancer. 2001;91:2110-2121. (Pubitemid 32476376)
75. Fink AM, Lass H, Hartleb H, et al. S-classification of sentinel lymph node predicts axillary nonsentinel node status in patients with breast cancer. Ann Surg Oncol. 2007;15:848-853.
76. Van Zee KJ, Manasseh DM, Bevilacqua JL, et al. A nomogram for predicting the likelihood of additional nodal metastases in breast cancer patients with a positive sentinel node biopsy. Ann Surg Oncol. 2003;10:1140-1151. (Pubitemid 40486808)
77. Kocsis L, Svebis M, Boross G, et al. Use and limitations of a nomogram predicting the likelihood of non-sentinel node involvement after a positive sentinel node biopsy in breast cancer patients. Am Surg. 2004;70:1019-1024.
78. Lambert LA, Ayers GD, Hwang RF. Validation of a breast cancer nomogram for predicting nonsentinel lymph node metastases after a positive sentinel node biopsy. Ann Surg Oncol. 2006;13:310-320. (Pubitemid 43255913)
79. Kohrt HE, Olshen RA, Bermas HR, et al. Bay Area SLN Study new models and online calculator for predicting non-sentinel lymph node status in sentinel lymph node positive breast cancer patients. BMC Cancer. 2008;8:66. (Pubitemid 351566658)
80. Specht MC, Kattan MW, Gonen M, Fey J, Van Zee KJ. Predicting nonsentinel node status after positive sentinel lymph biopsy for breast cancer: clinicians versus nomogram. Ann Surg Oncol. 2005;12:654-659. (Pubitemid 41126095)
81. Park J, Fey JV, Naik AM, Borgen PI, Van Zee KJ, Cody HS III. A declining rate of completion axillary dissection in sentinel lymph node-positive breast cancer patients is associated with the use of a multivariate nomogram. Ann Surg. 2007;245:462-468. (Pubitemid 46673143)
82. Degnim AC, Reynolds C, Pantvaidya G, et al. Nonsentinel node metastasis in breast cancer patients: assessment of an existing and a new predictive nomogram. Am J Surg. 2005;190:543-550. (Pubitemid 41306072)
83. Alran S, De Rycke Y, Fourchotte V, et al. Validation and limitations of use of a breast cancer nomogram predicting the likelihood of non-sentinel node involvement after positive sentinel node biopsy. Ann Surg Oncol. 2007;14:2195-2201. (Pubitemid 47174905)
84. Roberts CA, Beitsch PD, Litz CE, et al. Interpretive disparity among pathologist in breast sentinel node evaluation. Am J Surg. 2003;186:324-329. (Pubitemid 38368603)
85. Cserni G, Sapino A, Decker T. Discriminating between micrometastases and isolated tumor cells in a regional and institutional setting. Breast. 2005;103:358-367. (Pubitemid 40129296)
86. Cserni G, Bianchi S, Boecker W, et al. Improving the reproducibility of diagnosing micrometastases and isolated tumor cells. Cancer. 2005;103:358-367. (Pubitemid 40129296)
87. Turner RR, Weaver DL, Cserni G, et al. Nodal stage classification for breast carcinoma: improving interobserver reproducibility through standardized histologic criteria and image-based training. J Clin Oncol. 2008;26:258-263.
88. Cserni G. Histopathologic examination of sentinel nodes. Breast J. 2006;(suppl 12):S152-S156. (Pubitemid 44337462)
89. Viale G, Mastropasqua MG. Pathologic examination of the axillary sentinel lymph nodes in patients with early-stage breast carcinoma: current and resolving controversies on the basis of the European Institute of Oncology experience. Virchows Arch. 2006;448:241-247. (Pubitemid 43357638)
90. Weaver DL, Krag DN, Manna EA, et al. Comparison of pathologist-detected and automated computer assisted image analysis detected sentinel node micrometastases in breast cancer. Mod Pathol. 2003;16:1159-1163. (Pubitemid 37414211)
91. Mesker WE, Torrenga H, Sloos WC, et al. Supervised automated microscopy increases sensitivity and efficiency of detection of sentinel node micrometastases in patients with breast cancer. J Clin Pathol. 2004;57:960-964. (Pubitemid 39213948)
92. Norton LE, Komenaka IK, Emerson RE, Murphy C, Badve S. Benign glandular inclusions a rare cause of a false positive sentinel node. J Surg Oncol. 2007;95:593-596. (Pubitemid 47164667)
93. Mairano E, Mazzarol GM, Pruneri G, et al. Ectopic breast tissue as a possible cause of false positive axillary sentinel lymph node biopsies. Am J Surg Pathol. 2003;27:513. (Pubitemid 36368550)
94. Carter BA, Jensen RA, Simpson JF, Page DL. Benign transport of breast epithelium into axillary lymph nodes after biopsy. Am J Clin Pathol. 2000;113:259-265. (Pubitemid 30212557)
95. Diaz NM, Mayes JR, Vrcel V. Modes of benign mechanical transport of breast epithelial cells to axillary lymph nodes. Adv Anat Pathol. 2005;12:7-9. (Pubitemid 40614484)
96. Diaz NM, Cox CE, Ebert M, et al. Benign mechanical transport of breast epithelial cells to sentinel lymph nodes. Am J Surg Pathol. 2004;28:1641-1645. (Pubitemid 39564971)
97. Vanderveen KA, Ramsamooj R, Bold RJ. A prospective, blinded trial of touch prep analysis versus frozen section for intraoperative evaluation of sentinel lymph nodes in breast cancer. Ann Surg Oncol. 2008;15:2006-2011.
98. Motomura K, Nagumo S, Komoike Y, et al. Accuracy of imprint cytology for intraoperative diagnosis of sentinel node metastases in breast cancer. Ann Surg Oncol. 2008;247:839-842. (Pubitemid 351591520)
99. Arora N, Martins D, Huston TL. Sentinel node positivity rates with and without frozen section for breast cancer. Ann Surg Oncol. 2008;15:256-261.
100. Pugliese MS, Tickman R, Wang NP, Atwood M, Beatty JD. The utility of intraoperative evaluation of sentinel lymph nodes in cancer. Ann Surg Oncol. 2007;14:1024-1030.
101. Jeruss JS, Hunt KK, Xing Y. Is intraoperative touch imprint cytology of sentinel lymph nodes in patients with breast cancer cost effective? Cancer. 2006;107:2328-2336. (Pubitemid 44748515)
102. Krishnamurthy S, Meric-Bernstam F, Lucci A, et al. A prospective study comparing touch imprint cytology, frozen section analysis, and rapid cytokeratin immunostain for intraoperative evaluation of axillary sentinel lymph nodes in breast cancer. Cancer. 2009;115:1555-1562.
103. Carlson RW, McCormick B. Update: NCCN breast cancer clinical practice guidelines. J Natl Compr Canc Netw. 2005;3(suppl 1):S7-S11. (Pubitemid 44265387)